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Bioecological Drivers of Rabies Virus Circulation in a Neotropical Bat Community

DOI: 10.1371/journal.pntd.0004378

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Abstract:

Introduction In addition to the commonly accepted importance of the vampire bat in the maintenance and transmission of the rabies virus (RABV) in South America, RABV infection of other species is widely evidenced, challenging their role in the viral cycle. Methodology / Principles findings To identify the bioecological drivers of RABV circulation in neotropical bat communities, we conducted a molecular and serological survey on almost 1,000 bats from 30 species, and a 4-year longitudinal survey in two colonies of vampire bats in French Guiana. RABV was molecularly detected in a common vampire and in a frugivorous bat. The sequences corresponded to haematophagous bat-related strains and were close to viruses circulating in the Brazilian Amazon region. Species’ seroprevalence ranged from 0 to 20%, and the risk of seropositivity was higher in bats with a haematophagous diet, living in monospecific colonies and in dense forests. The longitudinal survey showed substantial temporal fluctuations, with individual waves of seroconversions and waning immunity. The high prevalences observed in bat communities, in most habitats and in species that do not share the same microhabitats and bioecological patterns, the temporal variations, and a rather short period of detectable antibodies as observed in recaptured vampires suggest (i) frequent exposure of animals, (ii) an ability of the infected host to control and eliminate the virus, (iii) more relaxed modes of exposure between bats than the commonly assumed infection via direct contact with saliva of infected animals, all of which should be further investigated. Conclusions / significance We hypothesize that RABV circulation in French Guiana is mainly maintained in the pristine forest habitats that may provide sufficient food resources to allow vampire bats, the main prevalent species, to survive and RABV to be propagated. However, on the forest edge and in disturbed areas, human activities may induce more insidious effects such as defaunation. One of the ecological consequences is the disappearance of resources for tertiary or secondary consumers. Populations of vampires may then shift to alternative resources such as cattle, domestic animals and humans. Therefore, a good forest status, allowing both a dilution effect in highly rich bat communities and the maintenance of large populations of medium-sized and large mammals used as prey by vampires, should prevent their migration to anthropized areas.

References

[1]  Vigilato MA, Cosivi O, Kn?bl T, Clavijo A, Silva HM. Rabies update for Latin America and the Caribbean. Emerg Infect Dis. 2013;19: 678–679. doi: 10.3201/eid1904.121482. pmid:23750499
[2]  Escobar LE, Peterson AT, Favi M, Yung V, Medina-Vogel G. Bat-Borne rabies in Latin America. Rev Inst Med Trop Sao Paulo. 2015;57: 63–72. doi: 10.1590/S0036-46652015000100009. pmid:25651328
[3]  Da Rosa ES, Kotait I, Barbosa TF, Carrieri ML, Brand?o PE, Pinheiro AS, et al. Bat-transmitted human rabies outbreaks, Brazilian Amazon. Emerg Infect Dis. 2006;12: 1197–1202. pmid:16965697 doi: 10.3201/eid1208.050929
[4]  Barbosa TF, Medeiros DB, Travassos Da Rosa ES, Casseb LM, Medeiros M, Pereira A de S, et al. Molecular epidemiology of rabies virus isolated from different sources during a bat-transmitted human outbreak occurring in Augusto Correa municipality, Brazilian Amazon. Virology. 2008;370: 228–236. pmid:17996263 doi: 10.1016/j.virol.2007.10.005
[5]  Schneider MC, Romijn PC, Uieda W, Tamayo H, da Silva DF, Belotto A, et al. Rabies transmitted by vampire bats to humans: an emerging zoonotic disease in Latin America? Rev Panam Salud Publica. 2009;25: 260–269. pmid:19454154 doi: 10.1590/s1020-49892009000300010
[6]  Rupprecht CE, Hanlon CA, Hemachudha T. Rabies re-examined. Lancet Infect Dis. 2002;2: 327–343. pmid:12144896 doi: 10.1016/s1473-3099(02)00287-6
[7]  Johnson N, Aréchiga-Ceballos N, Aguilar-Setien A. Vampire bat rabies ecology, epidemiology and control. Viruses. 2014;6: 1911–1928. doi: 10.3390/v6051911. pmid:24784570
[8]  Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, Rupprecht CE. Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science. 2010;329: 676–679. doi: 10.1126/science.1188836. pmid:20689015
[9]  Salmón-Mulanovich G, Vásquez A, Albújar C, Guevara C, Laguna-Torres VA, Salazar M, et al. Human rabies and rabies in vampire and non vampire bat species, Southeastern Peru, 2007. Emerg Infect Dis. 2009;15: 1308–1310. doi: 10.3201/eid1508.081522. pmid:19751600
[10]  Sodré MM, da Gama AR, de Almeida MF. Updated list of bat species positive for rabies in Brazil. Rev Inst Med Trop Sao Paulo. 2010;52: 75–81. pmid:20464127
[11]  de Almeida MF, Martorelli LFA, Sodré MM, Katakoaka PAG, de Rosa AR. Rabies diagnosis and serology in bats from the State of S?o Paulo, Brazil. Rev Soc Bras Med Trop. 2011;44: 140–145. pmid:21468481 doi: 10.1590/s0037-86822011005000011
[12]  Costa LJC, Andrade FAG, Uieda W, Martorelli LFA, Kataoaka PAG. Serological investigation of rabies virus neutralizing antibodies in bats captured in the eastern Brazilian Amazon. Trans R Soc Trop Med Hyg. 2013;107: 684–689. doi: 10.1093/trstmh/trt080. pmid:24100701
[13]  Condori-Condori RE, Streicker DG, Cabezas-Sanchez C, Velasco-Villa A. Enzootic and Epizootic Rabies Associated with Vampire Bats, Peru. Emerg Infect Dis. 2013;19: 1463–1469. doi: 10.3201/eid1909.130083
[14]  Torres C, Lema C, Gury Dohmen F, Beltran F, Novaro L, Russo S, et al. Phylodynamics of vampire bat-transmitted rabies in Argentina. Mol Ecol. 2014;23: 2340–2352. doi: 10.1111/mec.12728. pmid:24661865
[15]  Pereira Vieira LF, Gon?alves Pereira SRF, Carnieli P Jr., Tavares LCB, Kotait I. Phylogeography of rabies virus isolated from herbivores and bats in the Espírito Santo State, Brazil. Virus Genes. 2013;46: 330–336. doi: 10.1007/s11262-012-0866-y. pmid:23264105
[16]  Oliveira R de N, de Souza SP, Lobo RS, Castilho JG, Macedo CI, Carnieli P Jr, et al. Rabies virus in insectivorous bats: implications of the diversity of the nucleoprotein and glycoprotein genes for molecular epidemiology. Virology. 2010; 405: 352–360. doi: 10.1016/j.virol.2010.05.030. pmid:20609456
[17]  Albas A, de Almeida Campos AC, Bastos Araujo D, Seabra Rodrigues C, Sodré MM, Durigon EL, et al. Molecular characterization of rabies virus isolated from nonhaematophagous bats in Brazil. Rev Soc Bras Med Trop. 2011;44: 678–683. pmid:22231241 doi: 10.1590/s0037-86822011000600006
[18]  Guarino H, Castilho JG, Souto J, Oliveira R de N, Carrieri ML, Kotait K. Antigenic and genetic characterization of rabies virus isolates from Uruguay. Virus Res. 2013;173: 415–420. doi: 10.1016/j.virusres.2012.12.013. pmid:23318595
[19]  Delpietro H, de Diaz AM, Fuenzalida E, Bell JF. Determination of the rate of rabies attack in bats. Bol Oficina Sanit Panam. 1972;73: 222–230. pmid:4263044
[20]  Mungrue K, Mahabir R. The rabies epidemic in Trinidad of 1923 to 1937: an evaluation with geographic information system. Wilderness Envir Med. 2011;22: 28–36. doi: 10.1016/j.wem.2010.11.001
[21]  Blackwood JC, Streicker DG, Altizer S, Rohani P. Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats. Proc Natl Acad Sci USA. 2013;110: 20837–20842. doi: 10.1073/pnas.1308817110. pmid:24297874
[22]  Streicker DG, Recuenco S, Valderrama W, Benavides JG, Vargas I, Pacheco V, et al. Ecological and anthropogenic drivers of rabies exposure in vampire bats: implications for transmission and control. Proc R Soc B. 2012;279: 3384–3392. pmid:22696521 doi: 10.1098/rspb.2012.0538
[23]  George DB, Webb CT, Farnsworth ML, O’Shea TJ, Bowen RA, Smith DL, et al. Host and viral ecology determine bat rabies seasonality and maintenance. Proc Natl Acad Sci USA. 2011;108: 10208–10213. doi: 10.1073/pnas.1010875108. pmid:21646516
[24]  Streicker DG, Lemey P, Velasco-Villa A, Rupprecht CE. Rates of viral evolution are linked to host geography in bat rabies. PLOS Patho. 2012b;8: e1002720. doi: 10.1371/journal.ppat.1002720
[25]  Moreno J, Baer GM. Experimental rabies in the vampire bat. Am J Trop Med Hyg. 1980;29: 254–259. pmid:7369444
[26]  Aguilar-Setién A, Loza-Rubio E, Salas-Rojas M, Brisseau N, Cliquet F, Pastoret PP, et al. Salivary excretion of rabies virus in healthy vampire bats. Epidemiol Infect. 2005;133: 517–522. pmid:15966107 doi: 10.1017/s0950268805003705
[27]  Kobayashi Y, Sato G, Shoji Y, Sato T, Itou T, Miura Y, et al. Molecular epidemiological analysis of bat rabies viruses in Brazil. J Med Vet Sci. 2005;67: 647–652. doi: 10.1292/jvms.67.647
[28]  Velasco-Villa A, Orciari LA, Juarez-Islas V, Gómez-Sierra M, Padilla-Medina I, Flisser A, et al. Molecular diversity of rabies viruses associated with bats in Mexico and other countries of the Americas. J Clin Microbiol. 2006;44: 1697–1710. pmid:16672396 doi: 10.1128/jcm.44.5.1697-1710.2006
[29]  Constantine DG. Bat rabies and other lyssavirus infections. Reston, VA: U.S. Geological Survey Circular 1329; 2009. 68 Available from: National Wildlife Health Center; Madison, WI; RA644.R3C665.
[30]  Zargar UR, Chishti MZ, Ahmad F, Rather MI. Does alteration in biodiversity really affect disease outcome?–A debate is brewing. Saudi J Biol Sci. 2014;22: 14–18. doi: 10.1016/j.sjbs.2014.05.004. pmid:25561877
[31]  Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, et al. High-Resolution Global Maps of 21st-Century Forest Cover Change. Science. 2013;342: 850–855. doi: 10.1126/science.1244693. pmid:24233722
[32]  Henry M, Cosson JF, Pons JM. Modelling multi-scale spatial variation in species richness from abundance data in a complex neotropical bat assemblage. Ecol Model. 2010;221: 2018–2027. doi: 10.1016/j.ecolmodel.2010.05.011
[33]  Gilbert AT, Petersen BW, Recuenco S, Niezgoda M, Gómez J, Laguna-Torres VA, et al. Evidence of rabies virus exposure among humans in the Peruvian Amazon. Am J Trop Med Hyg. 2012;87: 206–215. doi: 10.4269/ajtmh.2012.11-0689. pmid:22855749
[34]  Direccion General de Epidemiologia. Brote de rabia silvestre en la comunidad nativa San Ramón- Yupicusa, distrito Imaza, provincia Bagua, Amazonas– 2011: Situación actual. Bol Epidemiol (Lima). 2011;20: 138–139.
[35]  Fahl WO, Carnieli P Jr, Castilho JG, Carrieri ML, Kotait I, Iamamoto K, et al. Desmodus rotundus and Artibeus spp. bats might present distinct rabies virus lineages. Braz J Infect Dis. 2012;16: 545–551. doi: 10.1016/j.bjid.2012.07.002. pmid:23146155
[36]  Fernandes ME, Costa LJ, Andrade FA, Silva LP. Rabies in humans and non-human in the state of Pará, Brazilian Amazon. Braz J Infect Dis. 2013;17: 251–253. doi: 10.1016/j.bjid.2012.10.015. pmid:23477765
[37]  Berger F, Desplanches N, Baillargeaux S, Joubert M, Miller M, Ribadeau-Dumas F, et al. Rabies risk: difficulties encountered during management of grouped cases of bat bites in 2 isolated villages in French Guiana. PLoS Negl Trop Dis. 2013;7: e2258. pmid:23826400 doi: 10.1371/journal.pntd.0002258
[38]  Meynard JB, Flamand C, Dupuy C, Mahamat A, Eltges F, Queuche F, et al. First human rabies case in French Guiana, 2008: epidemiological investigation and control. PLoS Negl Trop Dis. 2012;6: e1537. doi: 10.1371/journal.pntd.0001537. pmid:22363830
[39]  Sikes RS, Gannon WL, A. C. A. U. C. O. T. A. S. O. MAMMALOGISTS. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal. 2011;92: 235–253. doi: 10.1644/10-mamm-f-355.1
[40]  de Thoisy B, Richard-Hansen C, Goguillon B, Joubert P, Obstancias J, Winterton P, et al. Rapid evaluation of threats to biodiversity: human footprint score and large vertebrate species responses in French Guiana. Biodiv Conserv. 2010;19: 1567–1584. doi: 10.1007/s10531-010-9787-z
[41]  Gond V, Freycon V, Molino JF, Brunaux O, Ingrassia F, Joubert P, et al. Broad-scale spatial pattern of forest landscapes types in the Guiana shield. Int J Appl Earth Obs Geoinf. 2011;13: 357–367. doi: 10.1016/j.jag.2011.01.004
[42]  Paget D. Etude de la diversité spatiale des écosystèmes forestiers guyanais, Thèse de Doctorat de l’ENGREF, 1999, France.
[43]  Borisenko AV, Lim BK, Ivanova NV, Hanner RH, Hebert PDN. DNA barcoding in surveys of small mammal communities: a field study in Suriname. Mol Ecol Res. 2008;8: 471–479. doi: 10.1111/j.1471-8286.2007.01998.x
[44]  Charles-Dominique P, Brosset A, Jouard S. Les Chauves-souris de Guyane. Collection Patrimoines Naturels, Ed MNHN, Paris n°49.pp 172. 2001.
[45]  Dacheux L, Reynes JM, Buchy P, Sivuth O, Diop BM. A reliable diagnosis of human rabies based on analysis of skin biopsy specimens. Clin Infect Dis. 2008;47: 1410–1417. doi: 10.1086/592969. pmid:18937576
[46]  Ellison JA, Johnson SR, Kuzmina N, Gilbert A, Carson WC, VerCauteren KC, et al. Multidisciplinary approach to epizootiology and pathogenesis of bat rabies viruses in the United States. Zoonoses Public Health. 2013;60: 46–57. doi: 10.1111/zph.12019. pmid:23137052
[47]  Bourhy H, Reynes JM, Dunham EJ, Dacheux L, Larrous F, Huong VT, et al. The origin and phylogeography of dog rabies virus. J Gen Virol. 2008;89: 2673–2681. doi: 10.1099/vir.0.2008/003913-0. pmid:18931062
[48]  Delmas O, Holmes EC, Talbi C, Larrous F, Dacheux L, Bouchier C, et al. Genomic Diversity and Evolution of the Lyssaviruses. PLoS ONE. 2008;3: e2057. doi: 10.1371/journal.pone.0002057. pmid:18446239
[49]  Talbi C, Holmes EC, de Benedictis P, Faye O, Nakouné E, Gamatié D, et al. Evolutionary history and dynamics of dog rabies virus in western and central Africa. J Gen Virol. 2009;90: 783–791. doi: 10.1099/vir.0.007765-0. pmid:19264663
[50]  Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28: 2731–2739. doi: 10.1093/molbev/msr121. pmid:21546353
[51]  Nylander JAA. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, 2004.
[52]  Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61: 539–542. doi: 10.1093/sysbio/sys029. pmid:22357727
[53]  Bourhy H, Sureau P. Rapid fluorescent focus inhibitions test (RFFIT). In: Commission des Laboratoires de Référence et d’Expertise, editors. Méthodes de Laboratoire pour le Diagnostic de la Rage (in French); Institut Pasteur: Paris, France, 1990. pp. 191–193.
[54]  Reynes JM, Molia S, Audry L, Hout S, Ngin S, Walston J, et al. Serologic evidence of lyssavirus infection in bats, Cambodia. Emerg Infect Dis. 2004;10: 2231–2234. pmid:15663870 doi: 10.3201/eid1012.040459
[55]  Ellison JA, Gilbert AT, Recuenco S, Moran D, Alvarez DA, Kuzmina N, et al. Bat Rabies in Guatemala. PLoS Negl Trop Dis. 2014;8: e3070. doi: 10.1371/journal.pntd.0003070. pmid:25080103
[56]  López-Roig M, Bourhy H, Lavenir R, Serra-Cobo J. Seroprevalence dynamics of European bat lyssavirus type 1 in a multispecies bat colony. Viruses. 2014;6: 3386–3399. doi: 10.3390/v6093386. pmid:25192547
[57]  Almeida MF, Massad E, Aguiar EAC, Martorelli LFA, Joppert AMS. Neutralizing Antirabies Antibodies in Urban Terrestrial Wildlife in Brazil. J Wildl Dis. 2001;37: 394–398. pmid:11310897 doi: 10.7589/0090-3558-37.2.394
[58]  East ML, Hofer H, Cox JH, Wulle U, Wiik H, Pitra C. Regular exposure to rabies virus and lack of symptomatic disease in Serengeti spotted hyenas. Proc Natl Acad Sci USA. 2001;98: 15026–15031. pmid:11742089 doi: 10.1073/pnas.261411898
[59]  Araujo DB, Martorelli LA, Kataoka AP, Campos AC, Rodrigues CS, Sanfilippo LF, et al. Antibodies to rabies virus in terrestrial wild mammals in native rainforest on the north coast of S?o Paulo State, Brazil. J Wildl Dis. 2014;50: 469–77. doi: 10.7589/2013-04-099. pmid:24779464
[60]  R Core Team.R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013. ISBN 3-900051-07-0, URL .
[61]  Brosset A, Charles-Dominique P, Cockle A, Cosson JF, Masson D. Bat communities and deforestation in French Guiana. Can J Zool. 1996; 74: 1974–1982. doi: 10.1139/z96-224
[62]  de Thoisy B, Pavan AC, Delaval M, Lavergne A, Luglia T, Pineau K, et al. Cryptic diversity in Common Mustached bat Pteronotus cf parnellii (Mormoopidae) in French Guiana and in Brazilian Amapa. Acta Chiropterologica. 2014;16:1–13. doi: 10.3161/150811014x683228
[63]  Kissi B, Tordo N, Bourhy H. Genetic polymorphism in the rabies virus nucleoprotein gene. Virology. 1995;209: 526–537. pmid:7778285 doi: 10.1006/viro.1995.1285
[64]  Moratelli R, Dias D, Bonvicino CR. Estrutura e analise zoogeografica de uma taxocenose de morcegos no norte do Estado do Amazonas, Brasil. Chiroptera Neotropical. 2010;16: 661–671.
[65]  Price JL, Everard COR. Rabies virus and antibody in bats in Grenada and Trinidad. J Wildl Dis. 1977;13: 131–134. pmid:864845 doi: 10.7589/0090-3558-13.2.131
[66]  Mochizuki N, Kobayashi Y, Sato G, Hirano S, Itou T, Ito FH, et al. Determination and Molecular analysis of the complete genome sequence of two wild-type rabies viruses isolated from a haematophagous bat and a frugivorous bat in Brazil. J Vet Med Sci. 2011;73: 759–766. pmid:21301181 doi: 10.1292/jvms.10-0238
[67]  Salas-Rojas M, Sánchez-Hernández C, Romero-Almaraz ML, Schnell GD, Schmid RK, Aguilar-Setién A. Prevalence of rabies and LPM paramyxovirus antibody in non-hematophagous bats captured in the Central Pacific coast of Mexico. Trans Roy Soc Trop Med Hyg. 2004;98: 577–584. pmid:15289094 doi: 10.1016/j.trstmh.2003.10.019
[68]  Delaval M, Charles-Dominique P. Edge effects on frugivorous and nectarivorous bat communities in a neotropical primary forest in French Guiana. Rev Ecol. 2006;61: 343–352.
[69]  Gay N, Olival KJ, Bumrungsri S, Siriaroonrat B, Bourgarel M, Morand S. Parasite and viral species richness of Southeast Asian bats: fragmentation of area distribution matters. Int J Parasitol Parasites Wildl. 2014;3: 161–170. doi: 10.1016/j.ijppaw.2014.06.003. pmid:25161915
[70]  Turmelle AS, Olival KJ. Correlates of viral richness in bats (order Chiroptera). EcoHealth. 2009;6: 522–539. doi: 10.1007/s10393-009-0263-8. pmid:20049506
[71]  Bourhy H, Kissi B, Lafon M, Sacramento D, Tordo N. J. Antigenic and molecular characterization of bat rabies virus in Europe. Clin Microbiol. 1992;30: 2419–26.
[72]  Scheffer K, Carrieri ML, Albas A, dos Santos HCP, Kotait I, Ito FH. Rabies virus in naturally infected bats in the State of S?o Paulo, Southeastern Brazil. Rev Saúde Pública. 2007;41: 389–395. pmid:17515992 doi: 10.1590/s0034-89102007000300010
[73]  Serra-Cobo J, López-Roig M, Seguí M, Sánchez LP, Nadal J, Borras M, et al. Ecological factors associated with European bat lyssavirus seroprevalence in spanish bats. PLoS ONE. 2013;8: e64467. doi: 10.1371/journal.pone.0064467. pmid:23700480
[74]  Amengual B, Bourhy H, López-Roig M, Serra-Cobo J. Temporal dynamics of European bat Lyssavirus type 1 and survival of Myotis myotis bats in natural colonies. PLoS ONE. 2007;2: e566. pmid:17593965 doi: 10.1371/journal.pone.0000566
[75]  Amengual B, Bourhy H, López-Roig M, Serra-Cobo J. Active monitoring of EBLV infection in natural colonies of the mouse-eared Bat (Myotis myotis). Dev Biol (Basel). 2008;131: 547–553. doi: 10.1371/journal.pone.0000566
[76]  Kermack WO, G. A. Mckendrick AG. A contribution to the mathematical theory of epidemics. Part 3. In further studies of the problem of endemicity. Proc R Soc Lond (A) Mat. 1927;141: 92–122
[77]  Galetti M, Dirzo R. Ecological and evolutionary consequences of living in a defaunated world. Biol Cons. 2013;163: 1–6. doi: 10.1016/j.biocon.2013.04.020
[78]  LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci USA. 2003;100: 567–571. pmid:12525705 doi: 10.1073/pnas.0233733100
[79]  de Thoisy B, Richard-Hansen C, Peres CA. Impacts of subsistence game hunting on amazonian primates. In: Garber Paul A., Estrada Alejandro, Bicca-Marques Júlio César, Heymann Eckhard W. and Strier Karen B. (eds). South American Primates: Comparative Perspectives in the Study of Behavior, Ecology, and Conservation. 2009. Book Series Developments in Primatology: Progress and Prospects, Springer Press, Chap 15, pp 389–412.

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